Longitudinal study on the effects of growth-promoting and therapeutic antibiotics on the dynamics of chicken cloacal and litter microbiomes and resistomes

• DOI: 10.1186/s40168-021-01136-4
• Publication Date: 2021-08-28T18:04:39Z
• Authors: Chhedi Lal Gupta; Shlomo E. Blum; Karuppasamy Kattu...; Tali Daniel; Shelly Druyan; Roni Shapira; Oleg Krifucks; Yong-Guan Zhu; Xin-Yuan Zhou; Jian-Qiang Su; Eddie Cytryn
• Keywords: 2. Zero hunger; 0301 basic medicine; Staphylococcus aureus; Shotgun metagenomics; Research; Microbiota; QR100-130; Antimicrobial resistance; Antibiotic-resistant bacteria; Anti-Bacterial Agents; 3. Good health; Microbial ecology; 03 medical and health sciences; Broiler chickens; Cloaca; Drug Resistance, Bacterial; Escherichia coli; Animals; Microbiome; Longitudinal Studies; Chickens; Growth-promoting antibiotics

AbstractBackgroundTherapeutic and growth-promoting antibiotics are frequently used in broiler production. Indirect evidence indicates that these practices are linked to the proliferation of antimicrobial resistance (AMR), the spread of antibiotic-resistant bacteria from food animals to humans, and the environment, but there is a lack of comprehensive experimental data supporting this. We investigated the effects of growth promotor (bacitracin) and therapeutic (enrofloxacin) antibiotic administration on AMR in broilers for the duration of a production cycle, using a holistic approach that integrated both culture-dependent and culture-independent methods. We specifically focused on pathogen-harboring families (Enterobacteriaceae,Enterococcaceae, andStaphylococcaceae).ResultsAntibiotic-resistant bacteria and antibiotic resistance genes were ubiquitous in chicken cloaca and litter regardless of antibiotic administration. Environment (cloaca vs. litter) and growth stage were the primary drivers of variation in the microbiomes and resistomes, with increased bacterial diversity and a general decrease in abundance of the pathogen-harboring families with age. Bacitracin-fed groups had higher levels of bacitracin resistance genes and of vancomycin-resistantEnterococcaceae(totalEnterococcaceaecounts were not higher). Although metagenomic analyses classified 28–76% of theEnterococcaceaeas the commensal human pathogensE. faecalisandE. faecium, culture-based analysis suggested that approximately 98% of the vancomycin-resistantEnterococcaceaewere avian and not human-associated, suggesting differences in the taxonomic profiles of the resistant and non-resistant strains. Enrofloxacin treatments had varying effects, but generally facilitated increased relative abundance of multidrug-resistantEnterobacteriaceaestrains, which were primarilyE. coli. Metagenomic approaches revealed a diverse array ofStaphylococcusspp., but the opportunistic pathogenS. aureusand methicillin resistance genes were not detected in culture-based or metagenomic analyses.Camphylobacteriaceaewere significantly more abundant in the cloacal samples, especially in enrofloxacin-treated chickens, where a metagenome-assembledC. jejunigenome harboring fluoroquinolone and β-lactam resistance genes was identified.ConclusionsWithin a “farm-to-fork, one health” perspective, considering the evidence that bacitracin and enrofloxacin used in poultry production can select for resistance, we recommend their use be regulated. Furthermore, we suggest routine surveillance of ESBLE. coli, vancomycin-resistantE. faecalisandE. faecium, and fluoroquinolone-resistantC. jejunistrains considering their pathogenic nature and capacity to disseminate AMR to the environment.